Comparison of endothelial cell phenotypic markers of late-outgrowth endothelial progenitor cells isolated from patients with coronary artery disease and healthy volunteers

Tissue Engineering - Part A

Volumn 15, Issue 11, 2009, Pages 3473-3486

  Stroncek, John D ^a   Grant, Bryan S ^a   Brown, Melissa A ^a   Povsic, Thomas J ^b   Truskey, George A ^a   Reichert, William M ^a  

^a Duke University   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD; BLOOD VESSEL PROSTHESES; BLOOD VESSELS; DISEASES; ELECTRIC CONDUCTIVITY MEASUREMENT; NITRIC OXIDE; SELF ASSEMBLY; TISSUE ENGINEERING;

CORONARY ARTERY DISEASE; ENDOTHELIAL PROGENITOR CELLS; ENDOTHELIALIZATION; IN-VITRO; MORPHOLOGICAL CHARACTERISTIC; PERIPHERAL BLOOD; PHENOTYPIC MARKERS; SYNTHETIC MATERIALS; VASCULAR TISSUE ENGINEERING;

ENDOTHELIAL CELLS;

NITRIC OXIDE; VERY LATE ACTIVATION ANTIGEN 5; VITRONECTIN RECEPTOR;

ADULT; AGED; ANGIOGENESIS; ARTICLE; BLOOD SAMPLING; CELL ADHESION; CELL ISOLATION; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY DISEASE; ENDOTHELIUM CELL; FEMALE; FLOW CYTOMETRY; HEART CATHETERIZATION; HUMAN; HUMAN CELL; MALE; MORPHOLOGICAL TRAIT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; STEM CELL;

EID: 72649086983     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2008.0673     Document Type: Article

References (60)

1. Zilla, P., Deutsch, M., and Meinhart, J. Endothelial cell transplantation. Semin Vasc Surg 12, 52, 1999.
2. Tiwari, A., Salacinski, H.J., Hamilton, G., and Seifalian, A.M. Tissue engineering of vascular bypass grafts: role of endo-thelial cell extraction. Eur J Vasc Endovasc Surg 21, 193, 2001.
3. Jarrell B.E., Williams, S.K., Stokes, G., Hubbard, F.A., Car-abasi, R.A., Koolpe, E., Greener, D., Pratt, K., Moritz, M.J., Radomski, J., and Speicher, L. Use of freshly isolated capillary endothelial cells for the immediate establishment of a monolayer on a vascular graft at surgery. Surgery 100, 392, 1986.
4. Arts, C.H., Hedeman Joosten, P.P., Blankensteijn, J.D., Staal, F.J., Ng, P.Y., Heijnen-Snyder, G.J., Sixma, J.J., Verhagen, H.J., de Groot, P.G., and Eikelboom, B.C. Contaminants from the transplant contribute to intimal hyperplasia associated with microvascular endothelial cell seeding. Eur J Vasc Endovasc Surg 23, 29, 2002.
5. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., and Isner, J.M. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964, 1997.
6. Lin, Y., Weisdorf, D.J., Solovey, A., and Hebbel, R.P. Origins of circulating endothelial cells and endothelial outgrowth from blood. J Clin Invest 105, 71, 2000.
7. Gulati, R., Jevremovic, D., Peterson, T.E., Chatterjee, S., Shah, V., Vile, R.G., and Simari, R.D. Diverse origin and function of cells with endothelial phenotype obtained from adult human blood. Circ Res 93, 1023, 2003.
8. Hur, J., Yoon, C.H., Kim, H.S., Choi, J.H., Kang, H.J., Hwang, K.K., Oh, B.H., Lee, M.M., and Park, Y.B. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler Thromb Vasc Biol 24, 288, 2004.
9. Ingram, D.A., Mead, L.E., Tanaka, H., Meade, V., Fenoglio, A., Mortell, K., Pollok, K., Ferkowicz, M.J., Gilley, D., and Yoder, M.C. Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood. Blood 104, 2752, 2004.
10. Shi, Q., Rafii, S., Wu, M.H-D., Wijelath, E.S., Yu, C., Ishida, A., Fujita, Y., Kothari, S., Mohle, R., Sauvage, L.R., Moore, M.A.S., Storb, R.F., and Hammond, W.P. Evidence for circulating bone marrow-derived endothelial cells. Blood 92, 362, 1998.
11. Sieveking, D.P., Buckle, A., Celermajer, D.S., and Ng, M.K.C. Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 51, 660, 2008.
12. Urbich, C., Aicher, A., Heeschen, C., Dernbach, E., Hof-mann, W.K., Zeiher, A.M., and Dimmeler, S. Soluble factors released by endothelial progenitor cells promote migration of endothelial cells and cardiac resident progenitor cells. J Molec Cell Cardiol 39, 733, 2005.
13. Rehman, J., Li, J., Orschell, C.M., and March, K.L. Peripheral blood "endothelial progenitor cells" are derived from monocyte/macrophages and secrete angiogenic growth factors. Circulation 107, 1164, 2003.
14. Yoder, M.C., Mead, L.E., Prater, D., Krier, T.R., Mroueh, K.N., Li, F., Krasich, R., Temm, C.J., Prchal, J.T., and Ingram, D.A. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109, 1801, 2007.
15. Timmermans, F., Van Hauwermeiren, F., De Smedt, M., Raedt, R., Plasschaert, F., De Buyzere, M.L., Gillebert, T.C., Plum, J., and Vandekerckhove, B. Endothelial outgrowth cells are not derived from CD133+ cells or CD45+ hema-topoietic precursors. Arterioscler Thromb Vasc Biol 27, 1572, 2007.
16. Gulati, R., Jevremovic, D., Witt, T.A., Kleppe, L.S., Vile, R.G., Lerman, A., and Simari, R.D. Modulation of the vascular response to injury by autologous blood-derived outgrowth endothelial cells. Am J Physiol Heart Circ Physiol 2004;287, H512, 2004.
17. Timmermans, F., Plum, J., Yoder, M., Ingram, D., Vande-kerckhove, B., and Case, J. Endothelial progenitor cells: identity defined? J Cell Molec Med 13, 87, 2009.
18. Ingram, D.A., Mead, L.E., Moore, D.B., Woodard, W., Fe-noglio, A., and Yoder, M.C. Vessel wall-derived endothelial cells rapidly proliferate because they contain a complete hierarchy of endothelial progenitor cells. Blood 105, 2783, 2005.
19. Scheubel, R.J., Zorn, H., Silber, R.-E., Kuss, O., Morawietz, H., Holtz, J., and Simm, A. Age-dependent depression in circulating endothelial progenitor cells inpatients undergoing coronary artery bypass grafting. J Am Coll Cardioly 42, 2073, 2003.
20. Schmidt-Lucke, C., Rossig, L., Fichtlscherer, S., Vasa, M., Britten, M., Kamper, U., Dimmeler, S., and Zeiher, A.M. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 111, 2981, 2005.
21. Werner, N., Kosiol, S., Schiegl, T., Ahlers, P., Walenta, K., Link, A., Bohm, M., and Nickenig, G. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 353, 999, 2005.
22. Massa, M., Rosti, V., Ferrario, M., Campanelli, R., Ramajoli, I., Rosso, R., De Ferrari, G.M., Ferlini, M., Goffredo, L., Bertoletti, A., Klersy, C., Pecci, A., Moratti, R., and Tavazzi, L. Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood 105, 199, 2005.
23. Lambiase, P.D., Edwards, R.J., Anthopoulos, P., Rahman, S., Meng, Y.G., Bucknall, C.A., Redwood, S.R., Pearson, J.D., and Marber, M.S. Circulating humoral factors and endo-thelial progenitor cells in patients with differing coronary collateral support. Circulation 109, 2986, 2004.
24. Hirschi, K.K., Ingram, D.A., and Yoder, M.C. Assessing identity, phenotype, and fate of endothelial progenitor cells. Arterioscler Thromb Vasc Biol 28, 1584, 2008.
25. Broxmeyer, H.E., Srour, E., Orschell, C., Ingram, D.A., Cooper, S., Plett, P.A., Mead, L.E., and Yoder, M.C. Cord Blood Stem and Progenitor Cells. Methods Enzymol 419, 439-473
26. Anamelechi, C.C., Truskey, G.A., and Reichert, W.M. My-lar(TM) and Teflon-AF(TM) as cell culture substrates for studying endothelial cell adhesion. Biomaterials 26, 6887, 2005.
27. Brown, M.A., Wallace, C.S., Anamelechi, C.C., Clermont, E., Reichert, W.M., and Truskey, G.A. The use of mild trypsi-nization conditions in the detachment of endothelial cells to promote subsequent endothelialization on synthetic surfaces. Biomaterials 28, 3928, 2007.
28. Truskey, G.A., and Proulx, T.L. Relationship between 3T3 cell spreading and the strength of adhesion on glass and silane surfaces. Biomaterials 14, 243, 1993.
29. Lusska, A., Wu, L., and Whitlock, J.P., Jr. Superinduction of CYP1A1 transcription by cycloheximide. Role of the DNA binding site for the liganded Ah receptor. J Biol Chem 267, 15146, 1992.
30. Fuchs, S., Hermanns, M.I., and Kirkpatrick, C.J. Retention of a differentiated endothelial phenotype by outgrowth endo-thelial cells isolated from human peripheral blood and expanded in long-term cultures. Cell Tissue Res 326, 79, 2006.
31. Rozen, S., and Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, eds. Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ: Humana Press, 2000, pp. 365-386.
32. van der Loo, B., Fenton, M.J., and Erusalimsky, J.D. cyto-chemical detection of a senescence-associated [beta]-galac-tosidase in endothelial and smooth muscle cells from human and rabbit blood vessels. Exp Cell Res 241, 309, 1998.
33. Allen, J., Khan, S., Serrano, M., and Ameer, G. Characterization of porcine circulating progenitor cells: toward a functional endothelium. Tissue Eng Part A 14, 183, 2008.
34. Griese, D.P., Ehsan, A., Melo, L.G., Kong, D., Zhang, L., Mann, M.J., Pratt, R.E., Mulligan, R.C., and Dzau, V.J. Isolation and transplantation of autologous circulating endo-thelial cells into denuded vessels and prosthetic grafts: implications for cell-based vascular therapy. Circulation 108, 2710, 2003.
35. Kaushal, S., Amiel, G.E., Guleserian, K.J., Shapira, O.M., Perry, T., Sutherland, F.W., Rabkin, E., Moran, A.M., Schoen, F.J., Atala, A., Soker, S., Bischoff, J., and Mayer, J.E. Functional small-diameter neovessels created using endothelial progenitor cells expanded ex vivo. Nat Med 7, 1035, 2001.
36. Shirota, T., He, H., Yasui, H., and Matsuda, T. Human en-dothelial progenitor cell-seeded hybrid graft: proliferative and antithrombogenic potentials in vitro and fabrication processing. Tissue Eng 9, 127, 2003.
37. Shirota, T., Yasui, H., and Matsuda, T. Intralumenal tissue-engineered therapeutic stent using endothelial progenitor cell-inoculated hybrid tissue and in vitro performance. Tissue Eng 9, 473, 2003.
38. Guven, H., Shepherd, R.M., Bach, R.G., Capoccia, B.J., and Link, D.C. The number of endothelial progenitor cell colonies in the blood is increased in patients with angiographically significant coronary artery disease. J Am Coll Cardiol 48, 1579, 2006.
39. Thill, M., Strunnikova, N.V., Berna, M.J., Gordiyenko, N., Schmid, K., Cousins, S.W., Thompson, D.J.S., and Csaky, K.G. Late outgrowth endothelial progenitor cells in patients with age-related macular degeneration. Invest Ophthalmol Vis Sci 49, 2696, 2008.
40. Rosenman, J.E., Kempczinski, R.F., Pearce, W.H., and Sil-berstein, E.B. Kinetics of endothelial cell seeding. J Vasc Surg 2, 778, 1985.
41. Magometschnigg, H., Kadletz, M., Vodrazka, M., Gra-benwöger, M., Moritz, A., Grimm, M., Böck, P., Leukauf, C., Trubel, W., and Wolner, E. Changes following in vitro endothelial cell lining of ePTFE prostheses: late morphologic evaluation of six failed grafts. Eur J Vasc Surg 8, 502, 1994.
42. Melero-Martin, J.M., Khan, Z.A., Picard, A., Wu, X., Par-uchuri, S., and Bischoff, J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood 109, 4761, 2007.
43. Walter, D.H., Rittig, K., Bahlmann, F.H., Kirchmair, R., Silver, M., Murayama, T., Nishimura, H., Losordo, D.W., Asahara, T., and Isner, J.M. Statin therapy accelerates reendo-thelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 105, 3017, 2002.
44. Brooks, P.C., Clark, R.A., and Cheresh, D.A. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264, 569, 1994.
45. Davids, L., Dower, T., and Zilla, P. The lack of healing in conventional vascular grafts. In: Zilla P, Greisler H, eds. Tissue Engineering of Prosthetic Vascular Grafts. Austin, TX: RG Landes Company, 1999, pp. 3-44.
46. Ingram, D.A., Krier, T.R., Mead, L,E., McGuire, C., Prater, D.N., Bhavsar, J., Saadatzadeh, M.R., Bijangi-Vishehsaraei, K., Li, F., Yoder, M.C., and Haneline, L.S. Clonogenic en-dothelial progenitor cells are sensitive to oxidative stress. Stem Cells 25, 297, 2007.
47. Sieveking, D.P., Buckle, A., Celermajer, D.S., and Ng, M.K. Strikingly different angiogenic properties of endothelial progenitor cell subpopulations: insights from a novel human angiogenesis assay. J Am Coll Cardiol 51, 660, 2008.
48. Naseem, K.M. The role of nitric oxide in cardiovascular diseases. Mol Aspects Med 26, 33, 2005.
49. Dekker, R.J., Boon, R.A., Rondaij, M.G., Kragt, A., Volger, O.L., Elderkamp, Y.W., Meijers, J.C.M., Voorberg, J., Panne-koek, H., and Horrevoets, A.J.G. KLF2 provokes a gene expression pattern that establishes functional quiescent differentiation of the endothelium. Blood 107, 4354, 2006.
50. Lin, Z., Kumar, A., SenBanerjee, S., Staniszewski, K., Parmar, K., Vaughan, D.E., Gimbrone, M.A., Jr., Balasubramanian, V., Garcia-Cardena, G., and Jain, M.K. Kruppel-like factor 2 (KLF2) regulates endothelial thrombotic function. Circ Res 2005;96, e48, 2005.
51. Case, J., Mead, L.E., Bessler, W.K., Prater, D., White, H.A., Saadatzadeh, M.R., Bhavsar, J.R., Yoder, M.C., Haneline, L.S., and Ingram, D.A. Human CD34+ AC133+ VEGFR-2+ cells are not endothelial progenitor cells but distinct, primitive hematopoietic progenitors. Exp Hematol 35, 1109, 2007.
52. Veleva, A., Cooper, S., and Patterson, C. Selection and initial characterization of novel peptide ligands that bind specifically to human blood outgrowth endothelial cells. Biotechnol Bioeng 98, 306, 2007.
53. Massa, M., Campanelli, R., Bonetti, E., Ferrario, M., Marinoni, B., and Rosti, V. Rapid and large increase of the frequency of circulating endothelial colony-forming cells (ECFCs) generating late outgrowth endothelial cells in patients with acute myocardial infarction. Exp Hematol 37, 8, 2009.
54. Huang, L., Hou, D., Thompson, M.A., Baysden, S.E., Shelley, W.C., Ingram, D.A., March, K.L., and Yoder, M.C. Acute myocardial infarction in swine rapidly and selectively releases highly proliferative endothelial colony forming cells (ECFCs) into circulation. Cell Transplant 16, 887, 2007.
55. Deschaseaux, F., Selmani, Z., Falcoz, P-E., Mersin, N., Meneveau, N., Penfornis, A., Kleinclauss, C., Chocron, S., Etievent, J-P., Tiberghien, P., Kantelip, J-P., and Davani, S. Two types of circulating endothelial progenitor cells in patients receiving long term therapy by HMG-CoA reductase inhibitors. Eur J Pharmacol 2007;562, 111, 2007.
56. Xing, Z., Ryan, M.A., Daria, D., Nattamai, K.J., Van Zant, G., Wang, L., Zheng, Y., and Geiger, H. Increased hematopoietic stem cell mobilization in aged mice. Blood 108, 2190, 2006.
57. Aranguren, X.L., Verfaillie, C.M., and Luttun, A. Emerging hurdles in stem cell therapy for peripheral vascular disease. J Mol Med 87, 3, 2009.
58. Reyes, M., Dudek, A., Jahagirdar, B., Koodie, L., Marker, P.H., and Verfaillie, C.M. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109, 337, 2002.
59. Ross, J.J., Hong, Z., Willenbring, B., Zeng, L., Isenberg, B., Lee, E.H., Reyes, M., Keirstead, S.A., Weir, E.K., Tranquillo, R.T., and Verfaillie, C.M. Cytokine-induced differentiation of multipotent adult progenitor cells into functional smooth muscle cells. J Clin Invest 116, 3139, 2006.
60. Amatschek, S., Kriehuber, E., Bauer, W., Reininger, B., Meraner, P., Wolpl, A., Schweifer, N., Haslinger, C., Stingl, G., and Maurer, D. Blood and lymphatic endothelial cell-specific differentiation programs are stringently controlled by the tissue environment. Blood 109, 4777, 2007